Research

My lab's research spans several related areas of physiological ecology. We draw on the disciplines of physiology, microbiology, endocrinology, behavior, ecology,and evolution. Our general goal is to understand the physiological mechanisms that underlie organismal-level phenomena having to do with reproduction and survival. We are particularly interested in the diversity of solutions among species to common problems such as those having to do with energy utilization, social organization, reproduction and aging. We take a comparative approach to such questions, carried out within a phylogenetic framework.

Birds live significantly longer than mammals of the same body size, and a major focus of our lab is to understand the mechanisms that account for differences in longevity between species, and reconstruct the evolution of those differences. To do this, we take an integrative approach to examining hypothesized causes of aging and their interactions. Much of the lab research is aimed at identifying (1) the pattern of aging, that is which physiological traits, including oxidative damage, telomere length and immune function, covary with age, and (2) reconstructing the evolution of differences in longevity, by discovering how these traits are related to survivorship and reproductive success.

Telomeres are repeating sequences of DNA that cap each end of each chromosome and help maintain chromosomal integrity, but normally shorten with each round of DNA replication. Mark Haussmann and I have shown that the rate of telomere shortening is inversely related to maximum life span in birds. In the longest-lived birds such as this Leach’s storm-petrel, telomeres do not shorten with age, and may even increase in length. Long-lived birds maintain telomere length via sustained high activity of telomerase, a ribozyme complex capable of elongating telomeres.

Accumulation of oxidative damage, a potential root cause of senescence, depends on interactions between the production of reactive oxidative species, antioxidant capacity, and damage repair rates. In cooperation with Anne Bronikowski's lab, we are investigating how each of these varies with age within species, using a lab colony of zebra finches and between species, using various free-living bird species, to test the oxidative damage hypothesis.

Tree swallow are a valuable model organism for the study of aging, because they nest in easily accessible nest boxes, return to nest in the same vicinity year after year, and readily tolerate many experimental manipulations. Our field sites located near Ames, IA, and near Ithaca, NY (in collaboration with David Winkler of Cornell University) are both part of the Golondrinas de las Americanas, a hemisphere-wide effort to improve understanding of the biology of Tachycineta swallows. At each site all birds that occupy nest boxes are banded. We know ages of most adults, and we record the date eggs are laid, clutch size, nestling growth rate, fledging success, and track reproductive success throughout a bird's lifetime. We use these demographic data to determine how physiological traits of individual birds affect survival and reproductive success. For example, tree swallows with the longest telomeres at age-one have life spans nearly 3-fold greater than one-year-olds with the shortest telomeres.

Immunosenescence is the deterioration of immune function with age, which may increase susceptibility to infection, autoimmune disease and cancer. In tree swallows, we have shown that cellular immunity decreases with age, as does proliferation of T-lymphocytes in vitro in response to the T-cell mitogens. However, neither B-cell mediated immune response, plasma natural antibodies nor complement-mediated cell lysis change with age, so some, but not all, aspects of immune function show senescence. Our comparative study of four species of birds showed cell-mediated immunity was inversely correlated with life-span, consistent with evolutionary theory that predicts longer life-spans should be associated with greater investment in self-maintenance.

We continue to pursue a long-standing interest in the incubation biology of birds, particularly embryonic energetics and thermal biology. Periodic cooling of eggs occurs when parent birds must leave the nest to forage. Chris Olson used house wrens and zebra finches to determine how such cooling episodes prolong development and decrease the efficiency of converting the energy stored in yolk into new tissue, to better understand the consequences to developing offspring of variation in thermal environment and adult behavior.

The necessity to keep egg temperature within favorable limits constrains adult behavior of birds. Chris Olsen manipulated egg temperature in the wild in house wrens using Peltier heat exchangers placed below the nest cup. Incubating females stayed on the eggs longer and took shorter off bouts when eggs cooled more rapidly. Thermal constraints that affect both embryo development and adult time budgets are likely to determine the temporal and spatial limits for successful avian reproduction.

We also work on the effects of prolactin, vasoactive intestinal peptide and dopamine on incubation behavior in birds ranging from zebra finches to Adelie penguins. In penguins tactile feedback from the brood patch to the hypothalamus that blocks prolactin release when the eggs are lost and thus terminates incubation behavior in many birds is not active. Even when penguins must leave their nest to forage at sea for days to weeks, they still retain the prolactin-based drive to return to the colony and resume incubation.

Prolactin secretion is essential for successful reproduction. In zebra finches, the prolactin secreting cells of the anterior pituitary remain ready for action, even in non-breeding birds. That facilitates quick response to the sudden but unpredictable onset of favorable conditions for breeding that follow rainfall in their arid natural environment. In contrast, bird species from predictable environments, like most north temperate species, show regular annual cycles in prolactin secretion capability. This photograph is a midsagittal anterior pituitary section from a female zebra finch visualized using immunocytochemistry. Cells positive for prolactin fluoresce red and are localized to the cranial lobe, but extend caudally; those for growth hormone fluoresce green and are confined primarily to the caudal lobe.

Effects of Hormones and Condition on Breeding of Adélie Penguins in Antarctica

Some of my past research dealt with the physiological and hormonal correlates of individual variance in reproductive behavior and breeding success in free-living Adélie Penguins. My goal was to understand the proximate causes of individual behavior in order to shed light on the evolutionary bases of life history patterns. We tested competing hypotheses concerning reproductive competency and hormone levels vs. general body condition as proximate explanations for behavioral shifts through the season. Elevated prolactin provides the physiological underpinning for the long (many days) shifts that birds spend in attendance at the nest, as well as the return to the nest by a foraging birds after many days at sea. When one member of the pair fails to return, however, the incubating bird stays at the nest for as long as possible, but eventually abandons the nest as prolactin levels fall. corticosterone levels rise and the bird enters the starvation stage of fasting.

The avian egg has been called one of the most perfect creations of nature. Yet eggs come in a variety of sizes, shapes, colors, require different incubation periods and produce chicks of vastly different maturational states. We showed that the pattern of energy deposition in eggs differs radically between those species that produce altricial young (and cheap eggs) and those that produce precocial young (and expensive eggs). However, the way that egg energy is used, either for growth, maintenance or to serve as a residual energy store after hatching, does not vary systematically with developmental mode.

We have been particularly interested in the physiological mechanisms that facilitate the switch from courtship and aggressive behavior to parental behavior in animals. These two behaviors are facilitated by different hormones (testosterone versus prolactin), and we have investigated how social organization (group living versus solitary living) and environmental conditions affect the hormonal basis for behavior. In group-living Harris' hawks of the southwest deserts, adult male helpers have elevated testosterone during the courtship phase, but juvenile-plumaged helpers do not. After the eggs hatch, the adult-plumaged helpers have elevated prolactin and begin bringing food back to the nestlings.

Jerram Brown and I, working on Mexican jays in southeastern Arizona, found that the nonbreeders in these complex groups of jays have the same hormonal levels of prolactin as the breeders and that prolactin changes follow the same time course. This differs from the pattern in other birds that don't have helpers. In addition the level of prolactin is significantly higher in the cooperatively breeding Mexican jay than in sympatric, but non- cooperative western scrub-jay. This supports the hypothesis that natural selection has affected both physiology and behavior of these birds as related aspects of a complex suite of characters associated with cooperative breeding.